1298 Florida Entomologist 96(4) December 2013

ARGE XANTHOGASTER (: ): A NEW THREAT TO PLANTS IN MEGHALAYA, INDIA

1* 1 2 2 1 3 1 D. M. Firake , G. T. Behere , P. D. Firake , D. J. Rajkhoa , N. S. Azad Thakur , M. S. Saini , Z. Rahman 1 and S. V. Ngachan 1Division of Crop Improvement, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India

2Division of Natural Resource Management, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India

3Department of Zoology and Environmental Sciences, Punjabi University, Patiala, India

*Corresponding author: E-mail: [email protected]

Abstract

The ,Arge xanthogaster (Cameron) (Hymenoptera: Argidae), has recently emerged as a major pest of (Rosa spp. L; Rosales: Rosaceae) in Meghalaya and causes around 80% damage to wild and cultivated rose plants. This is a first report ofA. xanthogaster as a pest of roses in India. Adults cause ovipositional injuries (split shoots) and larval feeding often results in complete defoliation. The species is multivoltine. Studies on its life history in new habitat are given. Since this species belongs to a species complex of Arge in which species are difficult to distinguish, an attempt was made to develop a DNA barcode based on standard barcoding gene cytochrome oxidase I (COI) of the mitochondrial DNA of this species.

Key Words: emerging pest, Arge xanthogaster, rose, gregarious and hymenopteran pest

Resumen

El árgido, Arge xanthogaster (Cameron) (Hymenoptera: Argidae), ha surgido recientemente como una de las principales plagas de rosas (Rosa spp L; Rosales: Rosaceae) en Meghalaya y causa alrededor del 80% de daño a las plantas silvestres y cultivadas de rosa. Esto es el primer informe de A. xanthogaster como una plaga de rosas en la India. Los adultos causan lesiones (brotes divididos) al poner los huevos y la alimentación de las larvas a menudo resulta en una defoliación total. La especie es multivoltina. Se presentan estudios sobre su historia de vida en el nuevo hábitat. Puesto que esta especie pertenece a un complejo de especies de Arge en que las especies son difíciles de distinguir, se hizo un intento para desarrollar un código de barras de ADN sobre la base de los códigos de barras estándar gen citocromo oxidasa I (COI) del ADN mitocondrial de esta especie.

Palabras Clave: plagas emergentes, Arge xanthogaster, rosa, plaga gregario e himenóptero

Roses (Rosa spp. L.; Rosales: Rosaceae) are large genus of Argidae with over 300 recognized one of the world’s leading and most popular world species (Taeger et al. 2010). A number of flower crops of commercial importance. In India, species of Arge are associated with roses e.g., it is first in demand and popularity among culti- A. ochropus (Gmelin 1790), A. pagana (Panzer, vated flowers. A large number of attack 1798), A. nigrinodosa Motschulsky (Kawasaki rose plants at almost every stage, and sometimes et al. 2012), A. simlaensis (Cameron) (Mahmood they cause severe damage (Duraimurugan & Jag- & Ullah 2011), A. geei Rohwer (Jiansheng et al. adish 2011). Recently, a sawfly,Arge xanthogaster 1996), A. przhevalskii Gussakovskij (Ying & Yuan (Cameron 1876) (Hymenoptera: Argidae) (Figs. 1992) and A. fumipennis (F. Smith) (Chauhan et 1-6) has emerged as a major defoliator of roses in al. 2002). Seven species, including A. xanthogas- Meghalaya causing about 80-85% damage to wild ter, are very closely related and are collectively and cultivated rose plants. A significant increase considered as the “xanthogaster group” (Chen et in their population was observed during 2011-12. al. 2009) or “ochropa group” (Smith 1989), viz., A. The family Argidae includes a number of de- paganiformis Rohwer, A. pagana (Panzer, 1798), structive, multivoltine species. Arge Schrank is a A. luteiventris Cameron, A. brevigaster Wei, A. Firake et al.: Arge xanthogaster: An Emerging Rose Pest in India 1299

Figs. 1-6. Arge xanthogaster (Cameron, 1876). 1. Forewing of variant of Meghalaya; 2. Forewing of variant of Sikkim and Manipur. 3r-m = 3rd Cubital vein; A = Anal vein; B1-B2 = Brachial cells 1&2; C1-C4 = Cubital cells 1-4; D1-D3 = Discoidal cells 1-3; M = Medial cell; P = Postellan cell; R = Radial cell; S = Submedian cells; 3. Egg laying posture of female. Adult females possess a strong sawlike ovipositor, which is used to make parallel cuts in the fresh/tender shoots of the host plant; 4a and 4b. Eggs are oval shaped and yellow in color; 5. Eggs of in 2 longitudinal rows in a branch of a rose plant. Sawfly places eggs singly in 2 parallel longitudinal rows in slits in the young shoots; 6. First instar larvae feeding on rose leaf from the leaf edge. After hatching the neonates quickly start feeding and devour tender leaves on rose bushes. albocaudalica Wei & Yan et He, A. xanthogaster Materials and Methods Cameron and A. geei Rohwer. Arge xanthogaster Cameron has been reported Species identification was confirmed by an from Manipur, Sikkim and Uttar Pradesh states expert sawfly taxonomist, Dr. M. S. Saini (Pun- of India, but information on its hosts and its biol- jabi University, Patiala, Punjab state, India). ogy is lacking (Saini & Thind 1995). As per the Specimens were thoroughly examined for any existing primary literature and to our knowledge, kind of morphological variability among pres- the pest status of A. xanthogaster has not been ent specimens of sawfly of Meghalaya and those reported, and therefore, this is the first report of specimens previously collected from Manipur A. xanthogaster as a pest of roses from India. Be- and Sikkim states of India. Wing venation was cause of difficulties in identification of species of selected to explore variability among the present the xanthogaster group, we attempted to develop populations of Meghalaya and previous speci- a DNA barcode based on standard barcoding of mens of Manipur and Sikkim states. The illus- cytochrome oxidase I (COI) gene of the mitochon- trations were prepared with the aid of a zoom drial DNA of this species. Furthermore, proper stereoscopic binocular (Kyowa Getner DVZ-555 management strategies of an emerging pest are with maximum magnification of 90X) fitted with largely based on better understanding of their life an ocular grid in 1 eye piece. The inking of the cycle and behavior. Here, we thus report on the final drawings was done with Rottering black biology and damage of A. xanthogaster in Megha- ink. The illustrations were scanned at 600 dpi laya and on the development of a DNA barcode black and white, and mounted onto plates by that may be helpful in future identification. Adobe©Photoshop©8.0. 1300 Florida Entomologist 96(4) December 2013

For DNA extraction and PCR amplification, diam × 20 cm height) containing medium sized larvae were collected from infected rose plants rose plants (30 cm height) were kept in the nat- from 2 different locations and reared to adults ural environment (during Jun-Jul) and female in the laboratory. Four adults (2 from each lo- A. xanthogaster were allowed to lay eggs inside cation) were used for DNA extraction. Genomic the tender twigs. After 3 days, pots with rose DNA was extracted from whole adults (minus plants were brought to the laboratory and kept wings and head) using a DNeasy® Blood and in specially designed rearing cages (size: Tissue Kit (Qiagen, Cat. # 6950) and by follow- 45 × 45 × 45 cm, front and upper side covered ing the supplier’s instructions for tissue. with glass and the remaining 3 sides covered PCR amplifications were performed using stan- with fine insect proof nylon net) and photope- dard barcoding primers (LepF1 and LepR1) in a riod of 16:8 h L:D was maintained throughout 50 µL reaction volume consisting of 25.0 µL of 2X the rearing. Newly emerged larvae (Figs. 7-12) Fermentas PCR Master Mix (Fermentas, Cat. # were allowed to grow and develop to the pre- K0171); 2.5 µM of each of LepF1 (5’-ATTCAAC- pupal stage on these rose plants. Morphological CAATCATAAAGATATTGG-3’) and LepR1 (5’-TA- characters of each larval instar were recorded AACTTCTGGATGTCCAAAAAATCA-3’) primers by a digital microscope and larval weight was and 40-60 ng of template DNA. measured by a digital electronic balance (Met- PCR conditions had following profile: initial tler Toledo® AB analytical balance, Model denaturation at 94 °C for 2 min (1 cycle); 94 °C for AB104-S). After pupal formation, cocoons were 30 s, 50 °C for 40 s and 72 °C for 1 min (05 cycles); separated out and kept in large glass jars until 94 °C for 30 s, 50 °C for 40 s and 72 °C for 1 min adult emergence. Cotton soaked with water and (35 cycles) followed by a final extension cycle at 72 honey solution (30%) was provided to adults for °C for 10 min. The success of PCR amplification food. was confirmed by running out 10 µL of the post- After mating, 5 females were kept separately PCR volume along with 100 bp ladder (Fermen- inside specially developed rearing cages (45 × tas, Cat. # SM0241) on 1.5% agarose gels at 140 45 × 45 cm) and were allowed to lay eggs inside V for 30 min and stained with ethidium bromide the tender twigs of rose plants. Fresh and me- and visualized over a UV light illuminator. dium-sized rose plants were provided regularly The successful PCR amplicons (40 µL post- at 2-day intervals. The number of eggs laid per PCR) were sent for direct sequencing to the Chro- day was counted by a magnifying lens, and total mous Biotech Pvt. Ltd., Bangalore, India. For ac- life time fecundity was recorded. Rearing condi- curacy purpose, all the samples were sequenced tions during the experimental period were 23-25 from both the ends (5’ and 3’). The DNA sequences °C, 85-90% RH and 16:8 L:D. Observations on obtained were analyzed using Pregap4 and Gap4 incubation, larval period, pupal period, lifetime programs within the Staden Molecular Biology fecundity and adult longevity were recorded at analysis software (Staden et al. 1998). Nucleotide appropriate stages and times. sequences were aligned using the sequence align- ment program Clustal X (Thompson et al. 1997) Results and Discussion and were checked manually. Sequence identity was determined by BLASTN search (Altschul et Identification of the Sawfly al. 1997) against the nr DNA database deposited in GenBank. Fresh specimens from Meghalaya were identi- Life history studies were undertaken at fied by comparing genitalia of with previ- Umiam (N 25° 41' 01.91" and E 91° 54' 46.24" ) ously published reports of Saini & Thind (1995), and adjoining areas of the Ri-Bhoi District (mid and they were found to be Arge xanthogaster hills), Meghalaya State, India. This area receives (Cameron) (Argidae: Hymenoptera). annual rainfall of about 2,000 mm and its alti- tude varies from 1,000 to 1,100 m asl. In order Morphological Variation in A. xanthogaster of to quantify the infestation level, a separate scale Northeastern India was made on the basis of plant damage, 0-25%, 26-50%, 51-75% and 76-100% defoliation/dam- Arge xanthogaster was previously reported aged plants were designated scale I, scale II, scale from Manipur and Sikkim states of India by Saini III and scale IV, respectively. A total of 432 rose & Thind (1995) without mentioning host plant plants (both wild and garden) were selected ran- records. Some external morphological variations domly in the locality and observations were taken were observed in A. xanthogaster. In some indi- at monthly intervals. viduals, the bluish-black color of the abdominal Rearing was carried out in the IPM laborato- terga extends to the last segment and usually ry, Division of Crop Improvement (Entomology), the color of wings was dark brown or occasion- ICAR Research Complex of NEH Region, Umi- ally slightly lighter. In addition, a few differences am, Meghalaya, India (N 25.6532° E 91.8843°) were also observed in wing venation of A. xan- during 2010-12. About 20 small pots (20 cm thogaster obtained from Meghalaya (Figs. 1 and Firake et al.: Arge xanthogaster: An Emerging Rose Pest in India 1301

Figs. 7-12. Arge xanthogaster. 7. Larvae of feeding on rose leaves. Early larval instars are gregarious and feed heavily on leaves and flower buds. Slight disturbance of the larvae results in them curling the posterior of their bodies in a snake-like manner; 8a. Dorsal view of mature larva. Mature larvae turn yellow with black spots and feed individually. Full-grown larvae show aposematic body colors as well as pubescence; 8b. Ventral view of mature larva; 9. Cocoon. Mature larvae fall down to the ground and spin cocoons (dirty white in color) located on or in the soil; 10. Pupa of Arge xanthogaster; 11. Cocoons of Arge xanthogaster aggregated in a group; and 12. Dorsal view of an adult of Arge xanthogaster.

2). The nervulus of the forewing meets at the quencing gave good quality sequences for all tip of the anal cell, whereas in specimens from the samples. A final 641 bp sequence were used Sikkim and Manipur (Fig. 2) the same joins the for alignment after trimming the messy ends anal cell much before its tip. In specimens from (5’ and 3’) of the sequences. Due to the absence Meghalaya, the 2nd recurrent vein joins the 3rd of INDELs, alignment of all the sequences was cubital cell in the middle, whereas it is joined to straight forward. The SNPs (Single Nucleotide the first half of the 3rd cubital cell in case of the Polymorphisms) were not observed among all Sikkim and Manipur specimens. Furthermore, the 4 individual sequenced. BLASTN search of in specimens of Meghalaya, the basalis was al- 641 bp sequence as a query in NCBI yielded ma- most straight whereas in specimens of Sikkim ny possible targets corresponding to the 5’ end and Manipur it was distinctly curved in its basal of COI gene; and Arge nigripes (Accession num- half. These variations were found in almost all bers EF032285 and AF146680) showed the clos- the available (collected) specimens of A. xantho- est homology (88%, E value 0.0) to the query (A. gaster from the 3 above mentioned states. How- xanthogaster). Beside A. nigripes, other hits did ever, wing venation can vary in sawflies, but the not belong to the genus Arge. A representative populations exhibited no variation in genitalic sequence of A. xanthogaster has been deposited morphology. to the NCBI with accession number JX532103. Due to the absence of sequence information for Development of a DNA Barcode this gene (COI) in genbanks, the correct iden- tity of this species was not established at the DNA from all individuals tested in this study molecular level; however, the taxonomic and was amplified successfully. The standard insect molecular information generated and deposited DNA barcoding primers (LepF1 and LepF2) in genbank from this study certainly should be used in this study amplified the target 790 bp helpful for future molecular identification and fragment of COI gene of mtDNA. Direct se- confirmation of this species. 1302 Florida Entomologist 96(4) December 2013

Damage and Life History of Arge xanthogaster per yr have been found in the study region (n = 298). Females mate generally once during their During the peak infestation period (i.e., Jul life; however, parthenogenetic reproduction was and Aug), out of a total of 432 plant surveyed, also commonly observed. Pupal diapause has also 39.67%, 28%, 24% and 9.33% plants were found been observed and overwintering occurred from having 0-25% (Scale I), 26-50% (Scale II), 51-75% the end of Dec to early May. (Scale III) and 76- 100% (Scale IV) defoliation, The overall results revealed that A. xanthogas- respectively. Furthermore, about 22% of the rose ter was mainly observed from May to Dec; and plants were found completely damaged at the end from Jan to Apr it was diapausing in the pupal of Nov (by both defoliation and ovipositional in- stage. This schedule may be an adaptation to jury, i.e., split shoots) the severe winter (from mid-Dec to mid-Mar) Arge xanthogaster was active from May to Dec, in the region. The detailed biology of A. pagana and the maximum damage (80% larval damage) was studied by Roller (2006) in central Slovakia was found to occur from late Jul to Nov. Adult (about N 48°), who found that late Jul to early females possessed a strong sawlike ovipositor, Aug was its main flight period at this northern which was used to make parallel cuts in the latitude. fresh/tender shoots of the host plant (Fig. 3) and Zenghe et al. (1991) studied the life cycle of a in which they deposited yellow-colored oval eggs related sawfly,A. pagana and reported the follow- (Fig. 4). The eggs were placed singly in 2 longi- ing information on life cycle; incubation period (6- tudinal rows in slits (21.7 ± 2.83 mm long, n = 12 days), larval period (8.5-18 days), pupal period 386) within the young shoots (Fig. 5). Each slit (8-13.5 days) and adult longevity (1.5-9.5 days); contained 27 ± 2.13 eggs (n = 278). The color of the and this life cycle was more or less similar to that eggs changed gradually, turning brown or black of A. xanthogaster. Early instar larvae of A. xan- as the eggs matured. thogaster were gregarious and fed together. Sub- Mean incubation period was found to be 7.60 ± sequently during last mature stage, they became 0.16 days (n = 178). After hatching the neonates solitary. Bright coloration and gregariousness are quickly started to feed and began to devour ten- generally linked traits in insects (Guilford 1990; der leaves on rose bushes (Fig. 6). Early larval Ruxton & Sherratt 2006), and A. xanthogaster instars were gregarious and fed heavily on leaves had these traits. Similar characteristics have also and flower buds (Fig. 7). The young larvae were been reported in several other sawfly species (Lis- dark green and looked similar to lepidopteran ton et al. 2010), and other common pest species, caterpillars. Mature larvae (about 25 mm long) especially Lepidoptera (Fitzgerald 1995; Tullberg turned yellow with black spots and fed individu- & Hunter 1996; Reader & Hochuli 2003; Lytan & ally (Figs. 8a and 8b). In many cases, entire de- Firake 2012). These characteristics could aid in foliation led to heavy plant damage especially to avoiding increased risk of predation and parasit- the flower bearing branches. Larval development ism, which, occurs comparatively more frequently took 16.30 ± 0.21 days and passed through about under solitary conditions (Costa 1997; Firake et 5 or 6 larval instars (n = 430). al. 2012). In addition, gregariousness also im- Full-grown larvae showed aposematic body proves resource localization and assimilation colors as well as pubescence, which generally (Bryant et al. 2000; Fordyce 2003), better survi- provide protection from other invertebrates and vorship and improved growth rate (Allen 2010). predatory birds (Guilford 1990; Costa 1997). Ad- In addition to this, a slight disturbance to A. xan- ditionally, larvae curl and uplift their posterior thogaster larvae results in them curling their pos- portion in a snakelike manner, especially when terior body (in a snake-like manner), which may threatened. When mature, larvae descended to reinforce the effectiveness of the pubescence by the ground and spun cocoons (dirty white in color) producing a ‘hedgehog effect’. Similar behaviors in or on the soil (Fig. 9) and completion of pu- have been reported in A. pagana, and they are be- pation occurred inside the cocoon. The pupa was lieved to be anti-predator defense activities (Petre yellowish and exarate (Fig. 10). On occasion, full- et al. 2007). grown larvae came together and formed grouped Arge pagana produced 2 to 3 generations from cocoons (Fig. 11). The pupal stage lasted for 10.10 May to Oct, whereas A. ochropus had 1 or 2 gen- ± 0.23 days (n = 430). erations per yr (http://uknature.co.uk/A.pagana- The adults were entirely black, except for the info.html). However, in our study, A. xanthogaster abdomen which was yellowish orange with black produced 6 to 7 overlapping generations in a yr, lines on the dorsal surface (Fig. 12). However, in which were facilitated by the prolonged favorable the folded-wing condition, the sawfly appeared climate (mainly warm temperatures and ample completely black. Female adults with a longevity rainfall) of the region. Parthenogenesis is quite of 6.40 ± 0.16 days, laid around 187 ± 3.5 eggs widespread in sawflies (Ying 1992; Zhenghe et in 6 to 7 slits (n = 382). Overall, A. xanthogaster al. 1991; Sahragard & Heydari 2001; Mahmood took about 40.40 ± 0.76 days to complete a full life & Ullah 2011), and was observed in our study. cycle and around 6 to 7 overlapping generations Unlike other rose sawflies, for exampleA. rosae Firake et al.: Arge xanthogaster: An Emerging Rose Pest in India 1303

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